EGF, epithelium and Action of serotonergic drugs on calcium level 179
Action of serotonin antagonists on cytoplasmic calcium
levels in early embryos of sea urchin Lytechinus pictus
YURI B. SHMUKLER
1
*, GENNADY A. BUZNIKOV
1
and MICHAEL J. WHITAKER
2
1
N.K.Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia and
2
Department
of Physiological Sciences, The Medical School, University of Newcastle, Newcastle-upon-Tyne, United Kingdom
ABSTRACT Possible interaction of the serotonergic system with intracellular calcium mechanisms
was investigated using techniques of ratio imaging measurement of intracellular Ca
2+
and confocal
microscopy in cleaving embryos of sea urchin Lytechinus pictus. Some serotonin antagonists
specifically increase free intracellular Ca
2+
and evoke transient regression of the first cleavage furrow,
suggesting possible linkage of serotonergic and calcium mechanisms in the regulation of cellular
events during cleavage divisions. These effects were more pronounced in the experiments with
hydrophilic 5-HT-antagonists, quarternary ammonium salts that do not penetrate the cell membrane.
Thus, it appears that 5-HT-receptors which mediate these effects are localised on the cell membrane,
whereas previously studied receptors mediating the cytostatic action of lipophilic 5-HT-antagonists
are localised intracellularly.
KEY WORDS: serotonin, Ca
2+
, cleavage divisions, cytoskeleton, receptor
Int. J. Dev. Biol. 43: 179-182 (1999)
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*Address for reprints: N.K.Koltzov Institute of Developmental Biology, 26 Vavilov st., Moscow, 117808, Russia. FAX: (7 095) 135-3055. e-mail: ybshm@ibrran.msk.su
It is well known now that neurotransmitters are multifunctional substances
playing,inparticular,animportantroleinregulatoryeventsofembryogenesis,
including the pre-nervous stages of development (Buznikov, 1967, 1990;
Buznikov et al ., 1996). One of the most interesting peculiarities of pre-
nervous neurotransmitter systems, is the co-existence of intracellular and
plasma membrane neurotransmitter receptors (Buznikov, 1990; Shmukler,
1993; Buznikov et al ., 1996). Both types of receptors are functionally
coupled to various second messengers, including cyclic nucleotides
(Shmukler and Grigoriev, 1984; Shmukler et al ., 1986; Capasso et al .,
1988), phosphoinositides (Buznikov et al ., 1993), and Ca
2+
(Shmukler et
al ., 1986; Buznikov et al ., 1993, 1996, 1997). The present work is devoted
to the study of the direct effects of drugs related to one pre-nervous
neurotransmitter, 5-HT, on cytoplasmic Ca
2+
levels in early sea urchin
embryos.
Effects of 5-HT antagonists and agonists during the first cleavage
division
TIC methiodide (PPM antagonist of 5HT
3
-receptors) applied during the
first cleavage division (when cleavage furrow formation has already
started) in Fura-2-dextran-ratio imaging experiments, evoked a Ca
2+
-rise
in a dose-dependent manner (total of 41 experiments, Table 1, Fig. 1).
DMSO (0.5%), used as a solvent of neurochemicals, had no significant
effect (Table 1).
Using the confocal microscope, the increase of free intracellular Ca
2+
caused by IM methiodide (100 μM) was observed in all of 6 experiments
(intensity comparing to resting level increased by 45±6.4% with a latent
period of 30 sec) (Fig. 2a,b). By comparison with the data from ratio imaging
experiments, the rise in Ca
2+
-level corresponds to approximately 0.27±0.04
Short Contribution
Abbreviations used in this paper: 5-HT, 5-hydroxytryptamine, serotonin; EDTA,
ethylenediaminetetraacetic acid disodium salt; ASW, artificial sea water;
BAPTA/AM, 1,2-bis (2-Aminophenoxy) ethane-N,N,N,N-tetraacetic acid
acetoxymethyl ester; Ca
2+
(i)
, intracellular level of free calcium ions; Fura-2/
DX, Fura-2 dextran; CG-1/DX, Calcium Green-1 dextran; PIPES, piperazine;
N,N’, tetraacetic acid; D-600, methoxyverapamil; 5-HTQ, trimethylserotonin
methiodide; TIC, 3-tropanyl-indole-3-carboxylate hydrochloride
(tropisetron); TIC methiodide, 3-tropanyl-indole-3-carboxylate methiodide;
IM, inmecarb hydrochloride; IM methiodide, inmecarb methiodide; DMSO,
dimethylsulfoxide; EPM, substance, easily penetrating the cell membrane;
PPM, substance, poorly penetrating the cell membrane.
μM. The duration of intracellular free Ca2+ elevation was from 1.5 to 7 min.
Similar results were obtained in experiments with KYuR-14 methiodide
(PPM 5-HT-antagonist, 75 μM, 3 experiments.
Specificity of the effects of 5-HT-antagonists
5-HTQ (PPM 5HT
3
-agonist, 100 μM) administered 10-40 sec before
TIC methiodide (100 μM) significantly decreased the effect of the latter in
Fura-2-Dextran ratio imaging experiments (Table 2, Fig. 3), but only areas
under the peaks differed significantly. Preliminary data show that the
protective action of 5-HT (100 μM) was weaker than 5-HTQ.
In confocal microscope experiments, 5-HTQ (100 μM) administered 1
min before IM methiodide (100 μM) completely prevented Ca
2+
increase
in 2 out of 5 experiments, and left it in more or less unchanged form in
another 3 experiments. No significant effects of 5-HTQ (100 μM) itself were
observed.